Abstract
Enzyme histochemistry and immunocytochemistry were used to determine the distribution of neurons in the snail Helix aspersa which exhibited nicotinamide adenine dinucleotide phosphate (NADPH) diaphorase activity and/or immunoreactivity to nitric oxide synthase (NOS). NADPH diaphorase-positive cells and fibres were distributed extensively throughout the central and peripheral nervous system. NADPH diaphorase-positive fibres were present in all neuropil regions of the central and peripheral ganglia, in the major interganglionic connectives and in peripheral nerve roots. NADPH diaphorase-positive cell bodies were found consistently in the eyes, the lips, the tentacular ganglia and the procerebral lobes of the cerebral ganglia; staining of cell bodies elsewhere in the nervous system was capricious. The distribution of NOS-like immunoreactivity differed markedly from that of NADPH diaphorase activity. Small clusters of cells which exhibited NOS-like immunoreactivity were present in the cerebral and pedal ganglia; fibres which exhibited NOS-like immunoreactivity were present in restricted regions of the neuropil of the central ganglia. The disjunct distributions of NADPH diaphorase activity and NOS-like immunoreactivity in the neurvous system of Helix suggest that the properties of neuronal NOS in molluscs may differ sigificantly from those described previously for vertebrate animals.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adam-Vizi V, Allen JTA, Baker PF (1988) The effects of nitroprusside and putative agonists on guanylate cyclase activity in squid giant axons. Biochim Biophys Acta 938:461–468
Anderson CR, Edwards SL, Furness JB, Bredt DS, Snyder SH (1993) The distribution of nitric oxide synthase-containing autonomic preganglionic terminals in the rat. Brain Res 614:78–85
Bredt DS, Snyder SH (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci USA 87:682–685
Bredt DS, Glass CE, Hwang PM, Fotuhi M, Dawson TM, Snyder SH (1991) Nitric oxide synthase protein and mRNA are discretely localised in neuronal populations of the mammalia CNS together with NADPH diaphorase. Neuron 7:615–624
Chapman PF, Atkins CM, Allen MT, Haley JE, Steinmetz JE (1992) Inhibition of nitric oxide synthase impairs two different forms of learning. NeuroReport 3:567–570
Chang JJ, Gelperin A (1980) Rapid taste aversion learning by an isoltaed molluscan central nervous system. Proc Natl Acad Sci USA 77:6204–6206
Chase R, Kamil R (1983) Neuronal elements in snail tentacle as revealed by horseradish peroxidase backfilling. J Neurobiol 14:29–42
Chiang C-H, Gabella G (1986) Quantitative study of ganglion neurons of the mouse trachea. Cell Tissue Res 246:243–252
Cooke IRC, Delaney K, Gelperin A (1985) Complex computation in a small neural network. In: Weinberger NM, McGaugh JL, Lynch G (eds) Memory systems of the brain. Guilford Press, New York, pp 173–191
Culligan N, Gelperin A (1983) One-trial associative learning by an isolated molluscan CNS: use of different chemoreceptors for training and testing. Brain Res 266:319–327
Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Snyder SM (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci USA 88:7797–7801
Delaney K, Gelperin A (1986) Post-ingestive food-aversion learning to amino acid deficient diets by the terrestrial slug Limax maximus. J Comp Physiol [A] 159:281–295
Dorsett DA (1986) Brains to cells: the neuroanatomy of selected gastropod species. In: Willows AO (ed) The mollusca, vol 9. Neurobiogy and behaviour, part 2. Academic Press, Orlando, pp 101–187
Dun NJ, Dun Sl, Wu SY, Förstermann U, Schmidt HHHW, Tseng LF (1993) Nitric oxide synthase immunoreactivity in the rat, mouse, cat and squirrel monkey spinal cord. Neuroscience 54:845–857
Elofsson R, Carlberg M, Moroz L, Nezlin L, Sakharov D (1993) Is nitric oxide (NO) produced by invertebrate neurones? NeuroReport 4:279–282
Elphick MR, Green IC, O'Shea M (1993) Nitric oxide synthesis and action in aninvertebrate brain. Brain Res 619:344–346
Förstermann U, Gorsky LD, Pollock JS, Schmidt HHHW, Heller M, Murad F (1990) Regional distrbution of EDRF/NO-synthesizing enzymes in rat brain. Biochem Biophys Res Comm 168:727–732
Gelperin A, Tank DW, Tesauro J (1989) Olfactory processing and associative memory: cellular and modeling studies. In: Byrne JH, Berry WO (eds) Neural models of plasticity: theoretical and empirical approaches. Academic Press, New York, pp 133–159
Gelperin A, Flores JA, Raccula-Behling F, Tank DW, Kleinfeld D (1993) Nitric oxide, extrinsic modulators and odors alter spatiotemporal dynamics in the olfactory network of Limax. Soc Neurosci Abs 19:336
Hölscher C, Rose SP (1992) An inhibitor of nitric oxide synthesis prevents memory formation in the chick. Neurosci Lett 145:165–167
Hope BT, Michael GJ, Knigge KM, Vincent SR (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 88:2811–2814
Li ZS, Furness JB (1993) Nitric oxide synthase in the enteric nervous system of the rainbow trout, Salmo gairdneri. Arch Histol Cytol 56:1–9
Li ZS, Furness JB, Young HM, Campbell G (1992) Nitric oxide synthase immunoreactivity and NADPH diaphorase enzyme activity in neurons of the gastrointestinal tract of the toad, Bufo marinus. Arch Histol Cytol 55:333–350
Li ZS, Young HM, Furness JB (1993) Nitric oxide synthase in neurons of the gastrointestinal tract of an avian species, Coturnix coturnix. J Anat (in press)
Moroz LL, Park J-H, Winlow W (1993) Nitric oxide activates buccal motor patterns in Lymnaea stagnalis. NeuroReport 4:643–646
Morris RGM, Anderson E, Lynch GS, Baudry M (1986) Selective impairment of learning and blockade of long-term potentiation by the N-methly-D-aspartate receptor antagonist, AP-5. Nature 319:774–776
O'Dell TJ, Hawkins RD, Kandell ER, Arancio O (1991) Tests of the roles of two difusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc Natl Acad Sci USA 88:11285–11289
Saffrey MJ, Hassall CJ, Hoyle CH, Belai A, Moss J, Schmidt HHHW, Förstermann U, Murad F, Burnstock G (1992) Colocalization of nitric oxide synthase and NADPH diaphorase in cultured myenteric neurons. NeuroReport 3:333–336
Sahley CL, Rudy JW, Gelperin A (1981) An analysis of associative learning in a terrestrial mollusc: higher-order conditioning, blocking and a transient US pre-exposure effect. J Comp Physiol 144:1–8
Scherer-Singler U, Vincent SR, Kimura H, McGeer EG (1983) Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J Neurosci Meth 9:229–234
Schmidt HHHW, Gagne GD, Nakane M, Pollock JS, Miller MF, Murad F (1992) Mapping of neuronal nitric oxide synthase in the rat suggests frequent co-localization with NADPH diaphorase but not with soluble guanylylcyclase, and novel paraneural functions for nitrinergic signal transduction. J Histochem Cytochem 10:1439–1456
Sheng H, Schmidt HHHW, Nakane M, Mitchell JA, Pollock JS, Förstermann U, Murad F (1992) Characterization and localization of nitric oxide synthase in non-adrenergic non-cholinergic nerves from bovine retractor penis muscles. Br J Pharmacol 106:768–773
Shuman EM, Madison DV (1991) A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254:1503–1506
Staubli U, Thibault O, DiLorenzo M, Lynch G (1989) Antagonism of NMDA receptors impairs acquisition but not retention of olfactory memory. Behav Neurosci 103:54–60
Vincent SR, Hope BT (1992) Neurons that say NO. Trends Neurosci 15:108–113
Young HM, Furness JB, Shuttleworth CW, Bredt DS, Snyder SH (1992) Co-localization of nitric oxide synthase immunoreactivity and NADPH diaphorase staining in neurons of the guinea-pig intestine. Histochemistry 97:375–378
Zs-Nagy I, Sakharov DA (1970) The fine structure of the protocerebrum of the pulmonate molluscs, Helix and Limax. Tissue Cell 2:399–411
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Cooke, I.R.C., Edwards, S.L. & Anderson, C.R. The distribution of NADPH diaphorase activity and immunoreactivity to nitric oxide synthase in the nervous system of the pulmonate mollusc Helix aspersa . Cell Tissue Res 277, 565–572 (1994). https://doi.org/10.1007/BF00300230
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00300230